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The Case for a Gaian Bottleneck: The Biology of Habitability

Article in Astrobiology · January 2016 DOI: 10.1089/ast.2015.1387

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Aditya Chopra Charley Lineweaver Australian National University Australian National University

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The Case for a Gaian Bottleneck: The Biology of Habitability

Aditya Chopra and Charles H. Lineweaver

Abstract

The prerequisites and ingredients for life seem to be abundantly available in the Universe. However, the Universe does not seem to be teeming with life. The most common explanation for this is a low probability for the emergence of life (an emergence bottleneck), notionally due to the intricacies of the molecular recipe. Here, we present an alternative Gaian bottleneck explanation: If life emerges on a planet, it only rarely evolves quickly enough to regulate greenhouse gases and albedo, thereby maintaining surface temperatures compatible with liquid water and habitability. Such a Gaian bottleneck suggests that (i) extinction is the cosmic default for most life that has ever emerged on the surfaces of wet rocky planets in the Universe and (ii) rocky planets need to be inhabited to remain habitable. In the Gaian bottleneck model, the maintenance of planetary habitability is a property more associated with an unusually rapid evolution of biological regulation of surface volatiles than with the luminosity and distance to the host star. Key Words: Life—Habitability—Gaia—Abiogenesis habitable zone (AHZ)—Circumstellar habitable zone (CHZ). Astrobiology 16, 7–22.

1. Fermi’s Paradox, Hanson’s Great Filter, our galaxy is because life’s emergence is difficult and rare. In and Bostrom’s Bottlenecks this case, humanity has already survived the biggest threat to its continued existence; the biggest bottleneck is behind us, e see no evidence that our galaxy has been colonized and we can relax. However, if we find life on Mars that has Wby an advanced technological civilization. Archae- evolved independently of life on Earth, this would be strong ological excavations have not unearthed alien spaceships, and evidence that there is no emergence bottleneck. If we find the optical and radio searches for extraterrestrial intelligence such life, Bostrom argues that the biggest bottleneck—the have not been successful (Tarter, 2001). If one assumes that self-destruction bottleneck—would then be in front of us. This once life emerges it evolves toward intelligence and techno- would be ‘‘by far the worst news ever printed on a newspaper logical civilizations, we are faced with Fermi’s paradox: cover.’’ As a plausible alternative to such catastrophic logic, Where is everybody? [Webb (2002), C´ irkovic´ (2009); but also we introduce the concept of a Gaian bottleneck, a bottleneck see Gray (2015) and Ward and Brownlee’s (2000) Rare Earth that life on Earth has already passed through. If such a bot- hypothesis]. To put this information in context, Hanson (1998) tleneck exists, the discovery of extant independently evolved introduced the concept of a Great Filter, describing the pos- martian life might be bad news, but the discovery of extinct sible bottlenecks in the assumed progression from molecular independently evolved martian life would not be. chemistry to life, from life to intelligence, and from intelli- In the standard view, the decrease in bombardment rate from gence to galactic colonization. If the emergence of life is a rare *4.5 to *3.8 Gya is associated with making Earth more and difficult process, then an emergence bottleneck could re- clement and thus enabling life to emerge and persist (Maher solve Fermi’s paradox. However, if technological civilizations and Stevenson, 1988). In contrast to this view, we postulate a inevitably destroy themselves, this self-destruction bottleneck Gaian bottleneck model in which early life (on Earth and could also resolve Fermi’s paradox. elsewhere) is not just a passive passenger but comes under Bostrom (2008) argued that the Great Filter is a valuable strong selection pressure to actively modify and regulate its tool for assessing existential risks to humanity. If the biggest environment. The emergence of life’s abilities to modify its barrier in the Great Filter is the emergence bottleneck, then environment and regulate initially abiotic feedback mecha- we will find no independently evolved life on Mars, and the nisms (what we call Gaian regulation) could be the most sig- apparent absence of advanced technological civilizations in nificant factor responsible for life’s persistence on Earth.

Planetary Science Institute, Research School of Earth Sciences, Research School of Astronomy and Astrophysics, The Australian National University, Canberra, Australia.

7 8 CHOPRA AND LINEWEAVER

This highlights an important difference between physics- observations suggest that this sequence—the formation of based estimates of habitability and the more unpredictable terrestrial planets—is not a rare occurrence that needs special patterns of biological evolution on the highly unstable sur- initial conditions. There seems to be no rocky-planet-in-the- face environments of young terrestrial planets. For example, CHZ bottleneck responsible for reducing the probability for bombardment rates inevitably decrease in the circumstellar the emergence of life. habitable zones (CHZs) of stars, but the timescales for the evolution of Gaian regulation are probably unpredictable 2.2. No elemental or molecular ingredient bottleneck. and would not inevitably evolve rapidly (or at all). Thus, if Life on Earth is made of hydrogen, oxygen, carbon, ni- there is anything special about what happened on Earth to trogen, sulfur, and phosphorus: ‘‘HOCNSP’’ (Chopra et al., allow life to persist here, it might have less to do with the 2010). HOCNSP are among the most abundant atoms in the decreasing bombardment rate in the Hadean, or special Universe (Pace, 2001; Lodders et al., 2009; Lineweaver and chemical ingredients, or sources of free energy, or even a Chopra, 2012b). Since the elemental ingredients for life are rare recipe for the emergence of life. The existence of life on the most common elements in the Universe, it is not surprising Earth today might have more to do with the unusually rapid that the molecular ingredients of life are also common. biological evolution of effective niche construction and Of the elements in the Universe that form molecules, water Gaian regulation in the first billion years. Habitability and (H O) is the combination of the first and second most abun- habitable zones would then not only be a passive abiotic 2 dant elements. Water should be a common feature of rocky property of stellar and planetary physics and chemistry planets (Raymond et al., 2004, 2007; Elkins-Tanton, 2012). (such as stellar luminosity, initial water content, and de- Radial mixing during the epoch of oligarchic growth ensures creasing bombardment rate) but would also be a result of that some water-rich materials from beyond the snowline are early life’s ability to influence initially abiotic geochemical injected into the more water-poor material of the feeding cycles and turn them into the life-mediated biogeochemical zones of rocky planets in the CHZ. Thus, it is likely that Mars cycles that we are familiar with on the current Earth (Len- and Venus both started out, like Earth, hot from accretional ton, 1998; Lenton et al., 2004; Schneider, 2004; Falkowski energy and impacts and wet from impacts of large hydrous (5– et al., 2008; Kump et al., 2009). Without rapid evolution of 20% water) asteroids from the outer asteroid belt (Morbidelli Gaian regulation, early extinction would be the most com- et al., 2000, 2012) and other ‘‘wet’’ accretionary material mon fate of planetary life. Even if the emergence of life is a (Drake and Righter, 2002; Drake, 2005). Terrestrial planets in common feature of wet rocky planets throughout the Uni- other planetary systems are also likely to start with variable, verse, the Gaian bottleneck model suggests that inhabited non-negligible amounts of water. Earth-like planets would be rare. Current terrestrial life is built of monomers such as amino acids, fatty acids, sugars, and nitrogenous bases. Amino acids 2. If There Is an Emergence Bottleneck, link together to form proteins; fatty acids link to form lipids; It Is Probably ‘‘Recipe-Based’’ sugars link to form carbohydrates; and nitrogenous bases 2.1. No stellar bottleneck. No wet-rocky-planet combine with sugar and phosphate to make nucleotide mono- bottleneck. Sun-like stars and Earth-like mers, which link to form RNA/DNA (Lineweaver and Chopra, planets are common. 2012b). Thus, life on Earth emerged when available monomers linked together to make polymers. Amino acids and other or- If our Sun were the most uranium-rich star in the Galaxy, ganic monomers fall from the skies in carbonaceous chondrites. and if life on Earth were uranium-based (instead of carbon- We have no reason to believe that the availability of these based), then we would have good reason to believe that life monomers is somehow unique to Earth or the Solar System. (either its emergence or persistence, or both) requires a rare The flux of such organics was particularly high during the first kind of uranium-rich host star. However, we have been billion years of the formation of Earth, and we have no reason to unable to identify any significant differences between the believe that this will not be the case during the formation of Sun and other stars that could plausibly be connected with terrestrial planets in other planetary systems. The assortment of an increased probability of abiogenesis. Sun-like stars are organic compounds found in carbonaceous chondrites and the common in the Universe (Robles et al., 2008). Thus, there probable universality of early heavy meteoritic bombardments seems to be no stellar bottleneck responsible for reducing indicate that new planetary systems should also be supplied the probability for the emergence of life. with organic ingredients and be conducive to the synthesis of Over the past decade, estimates for the frequency of rocky prebiotic molecules (Ehrenfreund and Charnley, 2000; Herbst planets in, or near, the CHZ have increased (Howard et al., and van Dishoeck, 2009; Tielens, 2013). We expect all the 2012; Lineweaver and Chopra, 2012a; Bovaird and Line- ingredients of life as we know it (HOCNSP, water, amino acids, weaver, 2013; Fressin et al., 2013; Petigura et al., 2013; sugars, nucleic acids, HCN, and other organics) to be present Marcy et al., 2014; Bovaird et al., 2015; Burke et al., 2015). and available on wet rocky planets throughout the Universe. An Rocky planets in the CHZ are likely to be a common outcome ingredient bottleneck seems implausible. of planetary formation. This result is supported by observa- tional, theoretical, and computational models of rocky planet 2.3. No free energy bottleneck since photon- formation in which gas-rich protoplanetary disks evolve into and chemical redox–based energy dust disks in which planetesimals form and undergo oligar- sources are common. chic growth into planetary embryos as they differentiate into iron-nickel-rich cores, silicate mantles, and crusts dominated Life (here and elsewhere) needs to do something for a by incompatible lithophiles (Elkins-Tanton, 2012; Morbidelli living (Conrad and Nealson, 2001; Nealson and Rye, 2013). et al., 2012; Chambers, 2014; Hardy et al., 2015). Models and This living depends on extracting free energy from an GAIAN BOTTLENECK: THE BIOLOGY OF HABITABILITY 9 environment out of thermodynamic equilibrium (Branscomb England, 2013; Nisbet and Fowler, 2014; Sousa and Martin, and Russell, 2013). This extraction is based on catalyzing 2014). This weakness provides motivation for alternative redox reactions or absorbing photons (Kleidon, 2012). The explanations for the apparent paucity of life in the Universe. interiors of rocky planets throughout the Universe are denser The Gaian bottleneck hypothesis is one such alternative. and hotter than their surfaces. Thus, thermal gradients, As we learn more about the origin of life, we can begin to density gradients, and the fluid flows they drive, set up redox define an abiogenesis habitable zone (AHZ) where the re- potentials that can be exploited (Nisbet and Fowler, 2014). quirements for life’s emergence are met. Many initially wet The environmental factors that enabled abiogenesis on rocky planets in the CHZ may possess the necessary and Earth, such as the geochemical disequilibria between rocks, sufficient conditions to get life started (AHZ in Fig. 1). The minerals, aqueous species, and gases, are likely to be habitability requirements for the origin of life may be sub- ubiquitous on wet rocky planets throughout the Universe. In stantially different from, and more specific than, the re- addition, for planets in the CHZ, fusion in a nearby star quirements to maintain life on a planet (as in the difference shines *6000 K photons onto *300 K surfaces and enables between the need to have a spark plug to start an engine and metabolisms based on photon capture (Annila and Annila, a radiator to keep it from overheating). In Fig. 1, we have 2008; Lineweaver and Egan, 2008). assumed that the AHZ is not necessarily a subset of cur- rently inhabited planetary environments. 2.4. Recipe bottleneck? How ubiquitous are abiogenesis habitable zones? 3. Emergence Bottlenecks versus Gaian Bottlenecks With the absence of bottlenecks associated with stars, An emergence bottleneck is illustrated in Fig. 2. The left planets, ingredients, and sources of free energy, the only panel shows a hypothetical planet with non-evolving plan- other factor that could produce an emergence bottleneck etary conditions. The right panel shows a more plausible would be ‘‘recipe.’’ While we do not know the specifics of the planet that initially had some habitable regions but, through prebiotic chemistry and geochemical environments neces- volatile evolution or other transient factors, lost its surface sary for life to emerge (e.g., Orgel, 1998; Stu¨eken et al., water and evolved away from habitable conditions (e.g.,a 2013), the view that life will emerge with high probability on runaway greenhouse or runaway glaciated planet). Without Earth-like planets is shared by many scientists. Darwin significant abiotic negative feedback mechanisms, the sur- (1871) speculated that the environment, ingredients, and face environments of initially wet rocky planets are volatile energy sources needed for the origin of life could be common, and change rapidly without any tendency to maintain the when he wrote about life emerging in ‘‘some warm little pond habitability that they may have temporarily possessed as their early unstable surface temperatures transited through with all sort of ammonia and phosphoric salts, light, heat, electricity present, that a protein compound was chemically habitable conditions (Fig. 6C). formed, ready to undergo still more complex changes.’’ If there is no emergence bottleneck (Fig. 3), typical wet de Duve (1995) has been a more recent proponent of the rocky planets have initial conditions compatible with the view that the emergence of life is a cosmic imperative: emergence of life (AHZ). We postulate that almost all ini- ‘‘Life is either a reproducible, almost commonplace mani- tially wet rocky planets on which life emerges (left panel of festation of matter, given certain conditions, or a miracle. Fig. 3) quickly evolve like the abiotic planets represented in Too many steps are involved to allow for something in the right panel of Fig. 2. This unregulated evolution of between.’’ Discarding miracles, de Duve leaves us with life planetary environments away from habitable conditions as an ‘‘almost commonplace manifestation of matter.’’ As constrains the duration of life’s existence on the planet. We far as we know, Darwin’s warm little pond or de Duve’s call this early extinction of almost all life that ever emerges ‘‘certain conditions’’ are common on Earth-like planets and the Gaian bottleneck. In rare cases (for example on Earth), may be sufficient for the emergence of life. Biota throughout life will be able to evolve quickly enough to begin to reg- the Universe would emerge from chemistry through proto- ulate surface volatiles through the modification of abiotic biotic molecular evolution (e.g., Eigen and Winkler, 1992; feedbacks (right panel of Fig. 3). The potentially relevant Eschenmoser and Volkan Kisaku¨rek, 1996; Orgel, 1998; feedbacks involved in such early Gaian regulation are il- Ward and Brownlee, 2000; Martin and Russell, 2007; lustrated in Fig. 5 and discussed in Table 1 and Section 5. Russell et al., 2013). There is some tension between this conclusion and the 4. Early Extinction from Impacts and Devolatilization inability of synthetic biologists to produce life, despite having 4.1. Bombardment, impact frustration, and extinction access to a wide variety of ingredients, environmental setups, and energy sources. Plausible explanations for this tension During the late phases of Earth’s accretion (*4.5 to include (1) there is an emergence bottleneck due to a con- *4.0 Gya), episodes of cold ‘‘Norse ice-hell’’ were punc- voluted recipe whose requirements only rarely occur natu- tuated by brief periods of hot inferno with magma oceans rally; or (2) there is no emergence bottleneck—the recipe for (Nisbet, 2002; Elkins-Tanton, 2008). Frequent, large, ran- life is simple—but we are not as imaginative or as resourceful dom impacts produced wide-ranging, unstable temperatures. as nature, so we have not replicated the recipe in the relatively The largest impacts were so large that any life that did short time we have been investigating the origin of life. We emerge during the transitory habitable periods was probably conclude that the idea of an emergence bottleneck is still bombarded into extinction. These early bombardment- plausible. However, the evidence for it is getting weaker as we induced extinctions have been called the impact frustration find out more about the proto-biotic molecular evolution that of life (Maher and Stevenson, 1988; Sleep et al., 1989, led to the emergence of life on Earth (e.g., Benner, 2013; 2014; Davies and Lineweaver, 2005; Marchi et al., 2014). FIG. 1. The conditions needed for the origin of life are in the abiogenesis habitable zone, or AHZ. Inhabited environments (green) are a subset of planetary environments (blue). Both of these can change with time. The AHZ con- ditions are probably narrower than the broader conditions to which life can now adapt (‘‘in- habited environments’’). Through its manage- ment of the greenhouse and its partitioning of reductants and oxidants, the activity of life in- creases the range of inhabited environments (Nisbet et al., 2007). Hence, the green cylinder emerges out of the AHZ and gets broader with time. More specific reasons for this broadening include (1) the evolution of increasingly effi- cient catalytic enzymes offering tighter control over reaction rates; (2) the ability of new en- zymes to access the energy from different redox pairs providing larger jDGj values (Nealson and Conrad, 1999); and (3) the evolution of eco- systems (Smith and Morowitz, 2016), global- level niche construction, and global biogeo- chemical feedback cycles (see Section 5), which we refer to as the ‘‘evolution of Gaian regula- tion of the biosphere.’’ (Color graphics avail- able at www.liebertonline.com/ast)

FIG. 2. Emergence Bottleneck: planets on which life does not get started. Here, we show habitable conditions (yellow) and planetary environments (blue), from the time of planetary formation at the bottom to *6 billion years later at the top. Life will not emerge on either of these planets since their initial planetary environments do not overlap with the AHZ where life could get started. Both of these planets are initially habitable since their environments overlap with habitable conditions. Left panel: In this unrealistic, non-evolving model, planetary environments do not change with time. Habitable regions remain uninhabited because life does not get started. Such planets are uninhabited but remain habitable. Right panel: Parts of this evolving planet were habitable, but life does not emerge. The planet undergoes abiotic evolution and moves quickly away from habitability. We argue (Section 4.2) that evolution away from habitability is probably the default for initially wet rocky planets. We would find such planets to be uninhabited (and if older than *1 billion years, uninhabitable)—consistent with the idea that a planet has to be inhabited to remain habitable. (Color graphics available at www.liebertonline.com/ast)

10 GAIAN BOTTLENECK: THE BIOLOGY OF HABITABILITY 11

FIG. 3. The AHZ may be a very common subset of the environments of rocky planets that are wet during their first billion years. As in the left panel of Fig. 2, we assume that these planets are unregulated by any abiotic negative feedbacks and have no tendency to maintain habitability. We assume that life gets started on both of these planets, so there is no ‘‘emergence bottleneck’’ (Section 2) as there was in Fig. 2. Left panel: Life is unable to evolve rapidly enough to control runaway positive feedbacks. Gaian regulation does not emerge fast enough to maintain habitability. Thus, we have a ‘‘Gaian bottleneck.’’ We propose that most wet rocky planets are of this kind. Right panel: In rare cases (as on Earth), Gaian

regulation evolves fast enough to make it through the Gaian bottleneck and keep at least part of the planet habitable for billions of years. Biospheric regulation maintains the habitability of the planet until *5 billion years after formation, at which time, increasing stellar luminosity and loss of water cause life to go extinct. Extinction happens in both panels but much later in the right panel. This figure illustrates our hypothesis that the emergence and rapid extinction of life may be quite common (left) but that the emergence of life followed by the evolution of Gaian regulation and the long-term persistence of life could be quite rare (right). (Color graphics available at www.liebertonline.com/ast)

The early heavy bombardment of Earth decreased by more We postulate that the combination of heavy bombardment, than *13 orders of magnitude during this period (Bland, volatile evolution, and thermal instability almost always 2005; Ko¨berl, 2006; Fig. 6A). As the rate of planetary ac- conspires to eliminate incipient life before it has a chance to cretion slowed, the impact rate and the size of the largest evolve sufficiently to regulate initially abiotic global cycles. impactors decreased. We also postulate that, exceptionally, life on Earth was able Habitable conditions became, at least fleetingly, more to counter the effects of volatile evolution, thermal instability, available for life (Abramov and Mojzsis, 2009; Abramov and the general abiotic tendency to drift away from habit- et al., 2013). Impact heating may have provided strong se- ability. In other words, we argue that the same catastrophic lection pressure on early life to evolve into deep environ- events that life on Earth seems to have overcome usually lead ments to survive thermal perturbations (Sleep et al., 1989; to extinction. In the first billion years on a wet rocky planet in Nisbet and Sleep, 2001; Mat et al., 2008). the Universe, impacts and an inability to control surface en- We have no reason to believe that these processes are vironments are usually not just frustrating, but fatal. specific to Earth or to our solar system. The surfaces of Earth-sized rocky planets will undergo an early heavy 4.2. Water loss and tendency to evolve away bombardment that produces severe intermittent temperature from habitability pulses. A decreasing bombardment rate is likely to be a generic process that controls the emergence and early per- Liquid water is not easy to maintain on a planetary sur- sistence of life on wet rocky planets near the CHZs of host face. The initial inventory and the timescale with which stars throughout the Universe. As the bombardment rate water is lost to space due to a runaway greenhouse, or frozen decreases, these rocky planets cool down and can harbor, at due to ice-albedo positive feedback, are poorly quantified, least temporarily, habitable environments where life can but plausible estimates of future trajectories have been emerge from primordial soups, hydrothermal vents, or any made. On Earth, dissociation of water vapor by UV radia- other AHZ candidate. Whether life usually persists after this tion in the upper atmosphere is ongoing and will eventually emergence is what we are calling into question. (*1–2 billion years from now) lead to the loss of water from 12 CHOPRA AND LINEWEAVER the bioshell and the subsequent extinction of life on Earth the first half billion years after formation (Nisbet, 2002; Fig. (Caldeira and Kasting, 1992; Franck, 2000; Lenton and von 6B, 6C). There are two ways to influence the surface tem- Bloh, 2001; Franck et al., 2002; von Bloh et al., 2005). perature of a planet (Fig. 5): change the albedo (gray loops) In our solar system, Venus, Earth, and Mars are usually or change the greenhouse gas content of the atmosphere assumed to have started out in similar conditions: hot from (blue loops) (Kasting, 2012). The amount and the phases of accretion and wet from the impacts of aqueous bodies from the volatiles (H2O, CO2,CH4) of rocky planet atmospheres beyond the snowline. However, atmospheric evolution of these control both the albedo and greenhouse warming. Albedo planets diverged significantly (Kasting, 1988; Kulikov et al., and greenhouse warming, in turn, control the amount and 2007; Driscoll and Bercovici, 2013). The simplest interpreta- phases of the volatiles. Strong positive feedback cycles (left tion of the D/H ratios of Venus:Mars:Earth:Sun (2000:70:10:1) side of Fig. 5) may lead to both (i) runaway greenhouse is that (i) Venus has lost the vast majority of its H2O; (ii) Mars (temperatures too hot for life) with runaway loss of atmo- lost about 85% of its initial water content, and the rest froze into sphere (hydrogen loss and thus water loss) or (ii) runaway the polar ice-caps and subsurface permafrost (Kurokawa et al., glaciation (lowering the temperature and/or water activity to 2014; Villanueva et al., 2015); and (iii) Earth was able to keep a levels not conducive to life). larger fraction of its H2O(Popeet al., 2012; Fig. 4). However, the answer to the question ‘‘Why didn’t Earth 4.3. The implausibility of the carbonate-silicate undergo a runaway greenhouse like Venus or a runaway cycle (and other abiotic negative feedback) glaciation like Mars?’’ may have as much, or more, to do in the first billion years with life on Earth than with Earth’s distance from the Sun. The biotic mechanisms of how this preservation has In his original estimate of the continuous habitable zones, been achieved have been discussed in the context of the Hart (1979) considered runaway greenhouse and runaway Gaia hypothesis by Harding and Margulis (2010). The glaciation feedback but did not account for the negative early devolatilization of Earth-like planets around M stars feedback of silicate weathering on his models. The resulting due to an extended pre-main sequence period of high continuous habitable zone of 0.95–1.01 AU had such a narrow extreme UV flux (above the dissociation energy of water, width that he wrote: ‘‘It appears, therefore, that there are *5 eV) could apply to some extent to Earth-like planets probably fewer planets in our galaxy suitable for the evolution around more massive stars (Luger and Barnes, 2015; Tian, of advanced civilizations than has previously been thought.’’ 2015). Such a narrow CHZ could help solve Fermi’s paradox (e.g., The amount of water (and volatiles in general) deposited Webb, 2002, Solution 36, p. 158). More recent work has taken or devolatilized during the late accretion phase of rocky into account a stabilizing negative feedback loop associated

planet formation in the Universe is highly variable (Raymond with the recycling of CO2 by plate tectonics. Walker et al. et al., 2004, 2009) and can produce desert worlds (Abe et al., (1981) proposed a greenhouse gas–based negative feedback 2011), ocean worlds (Le´ger et al., 2003), and probably ev- process employing the carbonate-silicate cycle through the erything in between. Abiotic volatile evolution will be rapid, mechanism of silicate weathering. Increasing surface temper- stochastic, and hostage to the timing, mass, volatile content, atures increases the silicate weathering rate, freeing up more 2+ and impact parameters of the largest impactors and the run- Ca and other cations that combine with CO2 (via aqueous - away feedbacks they could induce. bicarbonate HCO3 ) to produce insoluble carbonates. Thus, We argue that abiotic habitable zones are available ini- when the temperature rises, more atmospheric CO2 is seques- tially and fleetingly to wet planets within a wide range of tered, and temperature decreases (Walker, 1985, and the blue orbital radii (*0.5 to *2 AU) because of the thermal in- negative feedback loop on the right side of Fig. 5). This abiotic stability of their surfaces. Wide-ranging unstable tempera- negative feedback is largely responsible for moving the outer tures could provide transitory abiotic habitable zones during edge of the CHZ from 1.01 AU, as estimated by Hart (1979), to

FIG. 4. Schematic illustration of the water loss caused by impacts and hydrogen escape. Hydrogen escape may entirely desiccate a rocky planet within a few billion years (Lovelock, 2005). Desiccation is inevitable as the host star luminosity increases, a cold trap is lost, and the stratosphere becomes moist (Lenton and von Bloh, 2001; O’Malley-James et al., 2015). (Color graphics available at www.liebertonline.com/ast) GAIAN BOTTLENECK: THE BIOLOGY OF HABITABILITY 13

FIG. 5. Early Abiotic Feedbacks. During the first billion years after the formation of Earth (or of Earth-like planets), abiotic positive feedbacks (left) can lead to runaway surface temperatures outside the habitable range (both too hot and too cold). These positive feedbacks lead to the loss of liquid water [either from hydrogen escape to space or condensation into ice (Fig. 4)]. Abiotic negative feedbacks (right) have been invoked to stabilize surface temperatures, but they may not be significant in the first billion years, hence the dashed lines and the question marks (Section 4.3). As life evolves, it can strengthen or weaken these initially abiotic geochemical feedback loops and turn them into biogeochemical cycles and feedback loops. Evolving life can insert itself into these feedbacks at the points labeled A, B, C, and D (Table 1 and Section 5). (Color graphics available at www.liebertonline.com/ast)

Table 1. Abiotic Feedback Processes Active during the First Billion Years of a Wet Rocky Planet’s History and Potential Biotic Enhancements of the Feedback Cycle

Feedback Mechanism Feedback type Potential biological mediation

Greenhouse Greenhouse gases (Ingersoll, 1969; Positive A (Catling et al., 2001; Kasting, 2012; Goldblatt Abe et al., 2011) et al., 2009; Harding and Margulis, 2010) Greenhouse Silicate weathering Negative? B (Lovelock and Whitfield, 1982; Schwartzman (Walker et al., 1981) and Volk, 1989; Catling et al., 2001; Rosing et al., 2006; Ho¨ning et al., 2014) Albedo Ice albedo (Budyko, 1969; Hoffman, Positive C (Harding and Margulis, 2010; Watson 1998; Kopp et al., 2005) and Lovelock, 1983) Albedo Low clouds (Abe et al., 2011) Negative? D (Rosing et al., 2010) the more modern, larger values of 1.5–1.7 AU (e.g.,Kasting erative or at least significantly less effective than today. This et al., 1993; Kopparapu et al., 2013). undermines the main negative feedback mechanism proposed Since the temperature-dependent carbonate-silicate cycle to stabilize surface temperature on wet rocky planets for the provides a negative feedback, it could have been responsible first billion years or so, when they are most likely to experience for the long-term stabilization of Earth’s surface temperature. runaway greenhouse or runaway glaciation due to high in- With a sufficiently high silicate weathering rate, even a lifeless ventories of primordial greenhouse gases, higher bombard- planet could remain habitable. However, since temperature- ment rates, and higher volcanism; hence, the ‘‘?’’ associated dependent silicate weathering requires sub-aerial weathering with this negative feedback loop in Fig. 5 and Table 1. of silicate rocks (either granitic or basaltic), the magnitude of Without this abiotic feedback cycle to extend the outer edge the negative feedback of silicate weathering is roughly pro- of the CHZ, the much narrower Hart-like continuously portional to the amount of sub-aerial continental crust. In the habitable zone (Fig. 6B) becomes more plausible. first billion years of Earth’s history, the fraction of the surface The other abiotic negative feedback on surface temperature of Earth where sub-aerial erosion would have been possible shown in Fig. 5 is associated with low clouds: higher temper- may have been extremely small (Flament et al., 2008; Abbot atures / more volatilization / more low-altitude clouds / et al., 2012; Dhuime et al., 2015). Flament et al. (2008) higher albedo / lower temperatures. Low clouds increase modeled the sub-aerial weathering as a function of time and albedo and decrease surface temperatures more than they estimated that in the late Archean (*2.5 Gya) 2–3% of the contribute toward raising the surface temperature because of Earth’s surface was sub-aerial continent. the greenhouse effect associated with clouds (Abe et al.,2011). The little continental crust present was largely submerged. This is problematic because increasing volatilization produces Thus, it is likely that early in Earth’s history the negative both more low-altitude clouds, which could cool Earth due to feedback of the carbonate-silicate cycle may have been inop- their higher albedo, and more high-altitude clouds, which could 14 CHOPRA AND LINEWEAVER

FIG. 6. Bombardment, habitable zones, and the Gaian bottleneck. (A) Early heavy bombardment precludes life for the first *0.5 billion years, indicated by red in all three panels. These impacts produce heat pulses and both deliver and remove volatiles (Elkins-Tanton, 2011). Thus, the amount of H2O at the surface is highly variable during this period. The phase of the H2O at the surface is also highly variable during this period because of impact-induced alternation between greenhouse warming and ice-albedo runaway. (B) The width of the CHZ is usually considered to be a function of physics and chemistry but is often computed without the largely uncertain influence of clouds and placed between Venus (0.7 AU) and Mars (1.5 AU). Here the blue region is from the work of Hart (1979), and the orange regions are based on estimates by Kopparapu et al. (2013) for the conservative (light orange) and optimistic (dark orange) limits. Life plays no role in these computations. The *30% increase in the luminosity of the Sun since its formation is responsible for the outward migration of the traditional CHZ and some of the narrowness of Hart’s continuously habitable zone. The yellow zone in (B) represents our speculative version of a short-lived abiotic habitable zone at the tail end of the impact-induced thermal instabilities shown in the first billion years of panel (C). The width of the abiotic habitable zone begins with a fairly wide range of semimajor axes but lasts only from *0.5 to *1 Gyr and then shrinks to zero. After *1 Gyr, rapid impact-induced thermal excursions diminish, and surface temperatures drift away and run away from habitability. Planets become devolatized because of the runaway greenhouse effect (top of panel C), and because liquid water condenses out into ice due to the runaway ice-albedo effect (bottom of panel C), with no abiotically stable zone between them. The early evolution of Gaian regulation may be the main feature responsible for maintaining the surface temperature of Earth within a habitable range for the past *4 billion years (Lovelock, 2000). (Color graphics available at www.liebertonline .com/ast) GAIAN BOTTLENECK: THE BIOLOGY OF HABITABILITY 15 have a stronger greenhouse effect than albedo effect and thus that can modify or regulate surface temperature and the increase surface temperatures (Goldblatt and Zahnle, 2011; hydrological cycle (e.g., Lenton, 1998; Nisbet et al., 2012). Leconte et al., 2013). For this reason, the effects of clouds are Life can evolve to enhance and regulate the feedback loops often considered the biggest source of uncertainty in global (biological mediation processes A–D in Fig. 5 and Table 1). climate models and thus the ‘‘?’’ associated with this cycle in Biologically mediated feedback loops are stabilizing or Fig. 5 and Table 1. Gaian (Ricklefs and Miller, 2000). For habitability to be While it may be possible to vary albedo and greenhouse maintained, life could down-regulate the positive runaway gases within some plausible range and construct a wide CHZ, feedback loops and enhance the negative feedback loops. without negative feedback, there is no justification for tuning On Earth, life began to modulate the greenhouse gas com- these abiotic variables to maintain habitability. We postulate position of the atmosphere as soon as life became wide- that the abiotic stabilizing feedbacks (two cycles on the right spread (Nisbet, 2002; Nisbet et al., 2012; Nisbet and Fowler, side of Fig. 5) were probably negligible on early Earth. In 2014; Johnson and Goldblatt, 2015). their absence, it is hard to understand how habitability would The use of the Gaia hypothesis in ecology was reviewed by have been maintained. Driverless cars do not stay on roads. Free and Barton (2007). They argued [in agreement with Without significant abiotic stabilization, we propose that the Dawkins (1982)] that selection for global stability is implau- most plausible default becomes the abiotic tendency to evolve sible. However, they defined a Probable Homeostatic Gaia away from habitability shown in Figs. 1 and 6C. model: a planet ‘‘with appropriate starting conditions for life Just because Earth is at 1 AU and has been inhabited for will probably generate a biosphere the lifespan of which will *4 billion years does not mean that there is a physics-based, be extended, rather than reduced, by life-environment feed- biology-independent, computable continuous habitable zone. back.’’ In their Probable Homeostatic Gaia model, a ‘‘network With thermal instability and increasing stellar luminosity, it is of life-environment interactions, largely dependent on the by- not clear that a physics-based continuously habitable zone product effects of evolved traits, leads to global stability.’’ even exists. There may be no range of orbital distances (or This biology-based global stability is what we call Gaian any region of multidimensional abiotic parameter space) for regulation. We are invoking its rapid evolution to stabilize the which the surface environments of initially wet rocky planets early volatile and thermal instabilities of wet rocky planets. have sufficiently strong abiotic negative feedback to maintain If Gaian regulation plays the dominant role in maintain- habitability. If this is the case, purely abiotic computations of ing liquid water at the surface (Harding and Margulis, a continuously habitable zone may be misleading, and Gaian 2010), then the width of the CHZ would depend more on the regulation becomes a plausible explanation for the continu- quirks of biological evolution than on the more deterministic ously inhabited habitable zone in which we find ourselves. physics and chemistry that can be more easily modeled. For

most rocky planets in the CHZ to remain habitable, they may have to be inhabited: ‘‘habitability depends on in- 5. The Biology of Habitability in the First Billion Years habitance and the width of the habitable zone is difficult to It is usually assumed that the CHZ is determined by abiotic characterize’’ (Goldblatt, 2015). physical parameters: stellar mass and luminosity, planetary In Gaian literature, it is usually proposed that Earth became a mass and atmospheric greenhouse gas composition, surface Gaian planet in the Proterozoic (*2.5 Gya) and has been one albedo, and sometimes clouds. More recently planetary spin, ever since (Harding and Margulis, 2010, p. 45). We are pro- orbital eccentricity, obliquity, and initial water content have posing that the onset of Gaian regulation could have occurred been added to the list of physical parameters (e.g.,Gaidoset al., more than a billion years earlier, for example, through the 2005; Gonzalez, 2005; Lammer et al., 2009; Gu¨del et al., 2014; production, consumption, and regulation of greenhouse active Shields et al., 2016). Here, we argue that these abiotic pa- gases such as H2,CO2,andCH4. If there is a biotic solution for rameters can fleetingly enable the emergence of life but cannot the faint early Sun paradox (Sagan and Mullen, 1972; Sagan maintain habitable surface conditions with liquid water. As the and Chyba, 1997; Feulner, 2012) based on higher concentra- early heavy bombardment subsides, strong selection pressure tions of CO2, on biotic methanogenesis, or on biotic albedo on life begins to regulate, control, and even dominate the regulation, then this solution would necessarily have evolved mechanisms that create or maintain the temperatures and quickly during the transient abiotic habitable zone (yellow pressures at the surface of a planet that allow liquid water. If so, regions in Fig. 6B, 6C) (Walker, 1985; Pavlov et al., 2003; then biology (rather than physics or chemistry) can play the Haqq-Misra et al., 2008; Rosing et al.,2010). most important role in maintaining habitability. In addition to the abiotic environmental changes (due to 6. Predictions and Tests of the Gaian bombardment and devolatilization), there could be a long Bottleneck Hypothesis struggle that starts early between life and an environment that does not, abiotically, stay habitable. Feedback between life After the early heavy bombardment, life emerges with and environment may play the dominant role in maintaining some probability on initially wet rocky planets in the CHZ. the habitability of the few rocky planets in which life has However, due to large impacts and unstable abiotic volatile been able to evolve Gaian regulation quickly. If life gets evolution with no tendency to maintain habitability, almost started on a planet, there are many potential ways in which all life goes extinct early—with the rare exceptions of life that life can regulate the mechanisms that create or maintain the has undergone unusually rapid evolution and obtained some temperatures and pressures needed for liquid water (Schneider level of Gaian regulation. The most significant predictions of and Boston, 1991; Schneider, 2004; Harding and Margulis, this Gaian bottleneck model can be seen in Fig. 7 by com- 2010). Gaia researchers propose that life on Earth evolved to paring panels A and B with C. In panels A and B, wherever become integrated into previously abiotic feedback systems life emerges, it persists for billions of years. Thus, it has time 16 CHOPRA AND LINEWEAVER

FIG. 7. Different bottleneck scenarios and their fossil predictions. (A) Emergence Bottleneck. Life rarely emerges even on wet rocky planets. Few planets will have life or even fossils of extinct life. On the few planets where life does emerge, it persists for billions of years. (B) No Emergence Bottleneck. Life emerges with high probability and usually persists for billions

of years. Thus, life will be abundant on planets throughout the Universe. There will be many planets where life persisted for billions of years and then went extinct. On the oldest uninhabited planets, fossils of complex life will be abundant. (C)Gaian Bottleneck. Life emerges with some probability (possibly quite high), but it goes extinct within a billion years (green). Alternatively, some small fraction of inhabited planets successfully pass through the Gaian bottleneck (light green). The Gaian bottleneck model predicts that the vast majority of the fossils in the Universe will be from extinct microbial life. (Color graphics available at www.liebertonline.com/ast) to evolve complex and perhaps multicellular forms. In panel on the surface of a planet may be a better biosignature than C, which illustrates the Gaian bottleneck model, almost all oxygen (Luger and Barnes, 2015). Thus, the measurement of emerging life goes extinct rapidly and therefore, does not exoplanetary surface temperatures compatible with liquid have time to evolve into more complex forms. However, even water could be an important part of future search for ex- planets with Gaian regulation will not be able to counter in- traterrestrial life. Remote detection of atmospheric chemical definitely the increasing luminosity due to stellar evolution equilibrium may soon develop into a mature science of (Caldeira and Kasting, 1992; Franck, 2000; Lenton and von remote biodetection (e.g., Lovelock and Kaplan, 1975; Bloh, 2001; Franck et al., 2002; von Bloh et al., 2005). Hence, Krissansen-Totton et al., 2016). The Gaian bottleneck model the extinction at *6 Gyr in all three panels. predicts that the vast majority of the atmospheres of old If we are able to find well-preserved, *3.8 to *4.3 terrestrial planets in the traditional abiotic CHZs of their billion-year-old rocks on Venus or Mars, then we may be able host stars will be in chemical equilibrium because they are to identify isotopic anomalies produced by biotic actions, in a uninhabited. Hence, atmospheres in chemical disequilibrium way analogous to how 12C/13C ratios are used to infer the will be rare except for young (t ( 2 Gyr) terrestrial planets. existence of the earliest life in Isua, Greenland (Ohtomo In a critique of Gaian logic, Dawkins (1982, p. 236) wrote: et al., 2014). Whether it evolved independently of life on Earth will be difficult to determine. If we find evidence of For the analogy [of the Earth as an organism] to apply extant life on Mars or Venus that had an origin independent strictly, there would have to have been a set of rival Gaias, of Earth life, then this would be evidence against both the presumably on different planets. Biospheres which did not develop efficient homeostatic regulation of their planetary Gaian bottleneck hypothesis and the emergence bottleneck. atmospheres tended to go extinct. The Universe would have The surface temperature and existence of liquid water at, to be full of dead planets whose homeostatic regulation or near, the surface could be predominantly due to Gaian systems had failed, with, dotted around, a handful of suc- regulation rather than abiotic negative feedback. Liquid cessful, well-regulated planets of which the Earth is one. water on the surface of the planet (particularly old planets) would then not just be a prerequisite for life but a bio- What Dawkins describes here is also a prediction of the signature (Gorshkov et al., 2004). Existence of liquid water Gaian bottleneck hypothesis. The Gaian bottleneck model GAIAN BOTTLENECK: THE BIOLOGY OF HABITABILITY 17 parallels evolution on Earth in that the vast majority Humanlike intelligence may be another member of (*99.9%) of species that have ever lived are now extinct; this class (Lineweaver, 2008). We are suggesting that the vast majority of planetary life has gone extinct. the evolution of a kind of life that can quickly and In the far future, we may be able to find evidence for effectively regulate the volatiles on the surface of the biogenic isotopic anomalies on the initially wet rocky planet on which it finds itself may be a quirky product planets around most stars. Since life does not persist for long of the biological evolution of life on early Earth. in the Gaian bottleneck model, it predicts a universe filled (4) Why should Gaian regulation be rare? Franck et al. with isotopic or microscopic fossils from the kind of life that (2002, 2001) concluded that there are *500,000 ‘‘sister can evolve in *1 billion years, not the fossils of larger Gaias’’ in the Milky Way Galaxy but then listed a number multicellular eukaryotes or anything else that would take of physical factors [e.g., those discussed by Ward and several billion years to evolve. Brownlee (2000)] that could reduce this estimate. Cockell (2014) divided all environments in the Universe (5) It could be that early heavy impacts almost always into three types: (1) uninhabitable, (2) uninhabited habitats, extinguish life and do not need any help from subse- or (3) inhabited habitats (Cockell, 2011; Zuluaga et al., quent volatile evolution away from habitability. In 2014). A prediction of the Gaian bottleneck (persistence-is- which case, Gaian regulation would have nothing to do hard) model is that (2) and (3) will be rare. This is unfor- with life’s early or late extinction. Evidence for this tunate for future colonization efforts since uninhabited, but would be an anomalously low impact rate on Earth habitable, planets are the most ethically appealing places— (compared to the early impact rates on other wet rocky autochthonous life would not have to be displaced. planets). If this were the case, there would be no ten- Our search for life beyond Earth may be thwarted by the dency for life to evolve and regulate its environment. short timescales over which planets may remain inhabited. If it In this context, Tyrrell (2013) suggested that ‘‘Lucky takes several billion years to develop radio telescopes, then the Gaia’’ as described by Free and Barton (2007) and the Gaian bottleneck ensures that the vast majority of life in the anthropic principle provide a better explanation for the Universe is either young and microbial, or extinct. Therefore, continued habitability of Earth than ‘‘Probable Gaia,’’ the Gaian bottleneck model is consistent with current SETI which we assume here. results and can help resolve Fermi’s paradox, although it is not If the probability of the emergence and persis- oneofthesolutionstotheparadoxlistedbyWebb(2002). tence of life on wet rocky planets were infinitesi- mally small and there were only one life-harboring 7. What Could Be Wrong with Our Argument? planet in the Universe, we would, of necessity, find ourselves on that planet. Therefore, our mere exis-

(1) Gaian regulation is a controversial idea. It is usually tence cannot be used to infer the probability of life invoked to explain the long-term stability of the elsewhere. Additionally, invoking a scenario in surface temperature of Earth, starting in the Protero- which persistent life on Earth is exceptional com- zoic (*2.5 Gya). So invoking early, pre-Proterozoic pared to other planets (as we do here) cannot be Gaia is even more controversial. criticized with an argument such as, if Gaian regu- (2) If estimates of sub-aerial continental crust (e.g.,by lation is rare, then we should not be here. Self- Flament et al., 2008) are significantly too low and selection overcomes this critique. there was abundant sub-aerial crust earlier than (6) One argument against early Gaian regulation is that *3.8 Gya (e.g., Van Kranendonk, 2010), then abiotic the unit of biological selection starts small and moves negative feedback based on the carbonate-silicate to larger groups as in the following chronological cycle could have stabilized surface temperatures very sequence: genes, chromosomes, single cells, colonies early in Earth’s history, without Gaian regulation. If of cells (bacterial mats), multicellular organisms, early continent formation is a common feature of colonies of multicellular organisms (superorganisms), rocky planets, then invoking Gaian regulation may be ecosystems of various sizes (which produce Gaian unnecessary to explain Earth’s early thermal stability. regulation only when they are widespread). In this (3) We are arguing that sequence, the evolution of Gaian regulation happens last. However, among the earliest life-forms we know (a) Gaian regulation evolved on Earth. of, stromatolites were already ecosystems of bacterial (b) The evolution of Gaian regulation is not common. mats (Walter et al., 1992). This could seem paradoxical, because to justify (a) (7) The Universe does not seem to be teeming with life. we have presented arguments making the emergence This could be an observational selection effect: it is of Gaian regulation plausible. These same arguments teeming with life, but we just have not been able to could suggest that Gaian regulation would be com- detect it yet. Even in the future when the remote mon. However, there is a large class of phenomena detection of biosignatures is possible, it will be dif- that did happen on Earth that are uncommon or ficult to detect subsurface life (Boston et al., 1992; nonexistent elsewhere. We can trace the evolution of Gaidos et al., 1999; Jones et al., 2011; McMahon these phenomena and explain how they evolved on et al., 2013) that does not interact with the planet’s Earth, but these explanations cannot be generalized. atmosphere and is completely sustained by free en- For example, the evolution of the English language ergy based on geochemical disequilibrium. This can be traced and understood and made plausible, but would undermine some of the motivation for the this plausibility cannot be turned into a generic ar- Gaian bottleneck model but not the other arguments gument for the evolution of English on other planets. presented here. 18 CHOPRA AND LINEWEAVER

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